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Ramularia Collo-Cygni Epidemic bioRxiv preprint doi: https://doi.org/10.1101/215418; this version posted November 7, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. The evolutionary history of the current global Ramularia collo-cygni epidemic Remco Stam1§, Hind Sghyer1*, Martin Münsterkötter4,5*, Saurabh Pophaly2%, Aurélien Tellier2,Ulrich Güldener3, Ralph Hückelhoven1, Michael Hess1§ 1Chair of Phytopathology, 2Section of Population Genetics, 3 Chair of Genome-oriented Bioinformatics Center of Life and Food Sciences Weihenstephan, Technische Universität München, Germany 4Functional Genomics and Bioinformatics, University of Sopron, Hungary 5Institute of Bioinformatics and Systems Biology, Helmholtz Zentrum München, Germany * contributed equally to this work § correspondence: Remco Stam: [email protected] Michael Hess: m.hess@ tum .de % current address: Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Sweden & Division of Evolutionary Biology, Faculty of Biology II, Ludwig-Maximilians-Universität München, Germany Abstract Ramularia Leaf Spot (RLS) has emerged as a threat for barley production in many regions of the world. Late appearance of unspecific symptoms caused that Ramularia collo-cygni could only by molecular diagnostics be detected as the causal agent of RLS. Although recent research has shed more light on the biology and genomics of the pathogen, the cause of the recent global spread remains unclear. To address urgent questions, especially on the emergence to a major disease, life-cycle, transmission, and quick adaptation to control measures, we de-novo sequenced the genome of R. collo-cygni (urug2 isolate). Additionally, we sequenced fungal RNA from 6 different conditions, which allowed for an improved genome annotation. This resulted in a high quality draft assembly of about 32 Mb, with only 78 scaffolds with an N50 of 2.1 Mb. The overall annotation enabled the prediction of 12.346 high confidence genes. Genomic comparison revealed that R. collo-cygni has significantly diverged from related Dothidiomycetes, including gain and loss of putative effectors, however without obtaining species-specific genome features. To evaluate the species-wide genetic diversity, we sequenced the genomes of 19 R. collo-cygni isolates from multiple geographic locations and diverse hosts and mapped sequences to our reference genome. Admixture analyses show that R. collo-cygni is world-wide genetically uniform and that samples do not show a strong clustering on either geographical location or host species. To date, the teleomorph of R. collo-cygni has not been observed. Analysis of linkage disequilibrium shows that in the world-wide sample set there are clear signals of recombination and thus sexual reproduction, however these signals largely disappear when excluding three outliers samples, suggesting that the main global expansion of R. collo-cygni comes from mixed or clonally propagating populations. We further analysed the historic population size (Ne) of R. collo-cygni using Bayesian simulations. We discuss how our genomic data and population genetics analysis can help understand the current R. collo- cygni epidemic and provide different hypothesis that are supported by our data. We specifically highlight how recombination, clonal spreading and lack of host-specificity could further support global epidemics of this increasingly recognized plant disease and suggest specific approaches to combat this pathogen. 1 bioRxiv preprint doi: https://doi.org/10.1101/215418; this version posted November 7, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Introduction: Plant pathogens cause serious damage on crop plants. They need to be controlled to achieve sufficient yield and best quality of the agricultural products. The ascomycete fungus Ramularia collo-cygni has been detected in barley samples worldwide [1]. The filamentous fungus is the major biotic agent of a leaf spotting complex [2] typically occurring late in the growing season on the upper canopy [3]. Ramularia leaf spot (RLS) poses a major risk in barley production, particularly in important barley growing regions like Scotland, mid Europe, Argentina and Uruguay It is estimated to cause losses up to 25 and in extreme cases up to 70% of the yield potential through a significant decrease of kernel size and quality [4]. Since thus far no major resistance genes were identified within the commercial barley genepool, control has been relying on the pre-epidemic use of several fungicides, but only a limited number of active substances are available and resistance has already been reported [5]. Ramularia collo-cygni was first described in 1893 by Cavara [6] as Ophiocladium hordei. However, it is only since the mid-1980’s that it became of increasing importance, with serious economic impact and the reasons for this remain unknown. Little is know about the pathogens biology or diversity in the field and e ven reproductive mode in the field and methods of dispersal remain largely unknown. Previously a draft genome had been published for R. collo-cygni strain DK05 [7]. The assembled 30.3 Mb genome data predicted 11,617 of gene models. It allowed the confirmation that R. collo-cygni belongs to the Dothidiomycetes, particularly to the family of Mycosphaerellaceae that contains several major plant pathogens. Additionally the study revealed relative paucity of plant cell wall degrading enzyme genes and a large number of secondary metabolite production associated genes. Both findings were hypothesised to be linked to the relatively long asymptomatic growth inside the host. The authors also highlighted the occurrence of several toxin encoding genes, on the genome, including the well-studied rubellins[8,9]. It is suggested that RLS-associated necrosis is caused by toxins produced by the fungus[9,10]. However, these toxins are non-host-specific and also present in other Dothideomycetes, thus their findings did not explain the recent emergence of the pathogen in barley.Instead it has been suggested that the intensive use of mildew resistant mlo-genotype cultivars might be one of the causes of the emergence of R. collo-cygni as a threat to barley production and quality. McGrann et al have investigated the trade-off between the barley mlo mutation-mediated powdery mildew resistance and susceptibility to RLS [11]. However, analysis of grain of near isogenic MLO and mlo-barley did subsequently not suggest enhanced levels of Rcc transmission via mlo-barley seed [12]. R. collo-cygni has also been isolated from wheat, oat, maize and from a number of uncultivated grasses such as Agropyron repens suggesting a broad host range [3] and shows microscopically similar compatible interactions with many of these grasses [13]. It is so far not known whether isolates of R. collo-cygni generally are able to infect a broad range of host species or if host specialization (e.g. to barley) occurs within local populations, nor do we have good insights in geographical diversity. An Amplified Fragment Length Polymorphism study investigating the population structure of samples from barley in Czechia, Slovakia, Germany and Switzerland showed variability between the samples and rejected the hypothesis of random mating in the field, but suggests that mixed reproduction is likely [14]. To date, no teleomorph of R. collo-cygni has been described. However data from both Amplified Fragment Length Polymorphism or microsatellites studies [15,16] also hint that sexual reproduction might take place in the field. Moreover, both studies show considerable variation between their two samples locations (Scotland & Denmark or Scotland & Czechia, respectively), but do not see clear substructures within the populations. Here we move beyond the genomics of R. collo-cygni and combine a comparative genomics approach with population genetics to get a deeper insight in R. collo-cygni’s biology and to better understand the life cycle as basis for sustainable control. We generated an independent draft genome and use this reference to gain a deeper understanding of the pathogens genome compared to selected model fungi and economically relevant plant pathogens, to identify those genetic factors that might contribute to its recent success. Moreover, we sequenced 17 additional isolates from a global collection from different hosts, to infer the pathogen’s population structure and its global diversity. Finally, we used our high quality assembly to infer the Linkage Disequilibrium, to 2 bioRxiv preprint doi: https://doi.org/10.1101/215418; this version posted November 7, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. define whether indeed R. collo-cygni is a sexual plant pathogen and to establish the historic population sizes of the pathogen. Our combined results show that R. Collo-cygni is unlike many other pathogens and that special care might be required to prevent worsening of the current epidemic. 3 bioRxiv preprint doi: https://doi.org/10.1101/215418; this version posted November 7, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Materials and Methods Fungal isolates and culture maintenance The isolate Urug2 (isolated in our laboratory from barley leaves collected in Uruguay) was used for the genome sequencing and expression analysis. It was stored in screw-cap test tubes that contained sterilized one fourth strength potato dextrose broth (¼PDB) (Carl Roth GmbH + Co. KG). Mycelium of the isolate was transferred to one fourth strength potato dextrose agar (¼PDA) (Carl Roth GmbH + Co.
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